CONTROL OF DEVELOPMENT IN CHENOPODIUM ALBUM L. BY SHADELIGHT: THE EFFECT OF LIGHT QUANTITY (TOTAL FLUENCE RATE) AND LIGHT QUALITY (RED.
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1 New Phytol. {\98l) S8, S 239 CONTROL OF DEVELOPMENT IN CHENOPODIUM ALBUM L. BY SHADELIGHT: THE EFFECT OF LIGHT QUANTITY (TOTAL FLUENCE RATE) AND LIGHT QUALITY (RED.FAR-RED RATIO) BY D. C. MORGAN AND HARRY SMITH Department of Botany, Adrian Building, University of Leicester, University Road, Leicester LEI 7RH U.K. {Accepted 4 September 1980) SUMMARY In nature, fluence rate and the red.far-red ratio are reduced in shadelight beneath vegetation; both show similar exponential decays with increasing canopy density. An assessment of the degree to which each of these factors controls development in natural shade was made by comparing Chenopodium album plants grown under vegetational shade with those grown under the controlled environment light treatments of low fluence rate, and combined low fluence rate and low red.far-red ratio. The observations of stem extension and specific leaf area from vegetational shade were entirely consistent with the eflfects of the controlled environment light treatments. The increase of specific leaf area in natural shade was probably due to the low fluence rate; the initial rapid stem extension in natural shade was probably due to the reduced red: far-red ratio. There is good evidence to suggest that the latter is a phytochrome-controlled phenomenon. INTRODUCTION Vegetational canopies act as selective absorption filters. Plants growing beneath or within them are, therefore, subjected to a light environment which diflfers from daylight in two characteristic respects; namely, low total photon fluence rate, and high proportion of far-red light (i.e. wavelength > 700 nm) (Yocum, Allen and Lemon, 1964; Vezina and Boulter, 1966; Holmes and Smith, 1977a, b; Tasker and Smith, 1977). The latter is usually described numerically as the red:far-red ratio, i.e. the ratio of photon fluence rates in 10 nm bandwidths centred on 660 nm and 730 nm, and has been called zeta {Q by Monteith (1976). For a wheat canopy in midsummer the fluence rate available for photosynthesis is reduced from approximately 1400 fimox m~^ s~^ in daylight to approximately 75 /imox m~^ s~^ in shadelight, whilst ^is reduced from approximately 11 in daylight to approximately 0-2 in shadelight (Holmes and Smith, 1975). Depending on the species and habitat, low fluence rate has been shown to increase leaf area ratio (Blackman and Wilson, 1951, 1954), increase leaf chlorophyll content (Jarvis, 1964), increase height (Grime and Jeffrey, 1965), decrease ribulose bisphosphate carboxylase activity, and increase the size of granal stacks (Bjorkman, 1968a, b). In many cases the degree to which a response is shown is systematically related to the species habitat. For example, the increase in leaf area ratio in low fluence rate is much greater in more shade tolerant species {Geum urbanum, Solanum dulcamara) than in shade intolerant species {Helianthus annuus, Trifolium subterraneum) (Blackman and Wilson, 1951). Such systematic relationships suggest that the response has significance for the ecology of the species as an adaptation to X/81/ $02.00/ The New Phytologist
2 24O D. C. MORGAN AND H. SMITH its habitat. The responses to low fluence rate appear to be particularly important as a mechanism for acclimating the photosynthetic apparatus to shadelight. The photoreceptor for these responses to fluence rate is unknown. A comprehensive change in developmental pattern is also shown by plants grown in low red:far-red ratio (Holmes and Smith, 1977c; McLaren and Smith, 1978). Again, some of these responses are systematically related to habitat - species from open habitats are more responsive than species which typically grow in vegetational shadelight (Morgan and Smith, 1979). The stem extension response to low red: far-red ratio is particularly striking. This may have significance for the ecology of the species - woodland plants cannot overtop the shading canopy and rapid stem extension would seriously weaken them; whilst for species which typically grow amongst herbaceous plants, shade avoidance by rapid stem extension is clearly advantageous. There is considerable evidence to suggest that the responses to low red.far-red ratio are under the control of the photoreceptor phytochrome (Smith and Holmes, 1977; Morgan and Smith, 1978; Morgan, O'Brien and Smith, 1980). In vegetational shadelight low fluence rate and low red:far-red ratio invariably occur together. The significance of either to the ecology of a species is therefore dependent on the way in which they interact to control development. In this paper we report the development of Chenopodium album, a shade intolerant annual weed, grown in: (1) the controlled environment in low fluence rate, (2) the controlled environment in combined low fluence rate and low red: far-red ratio, (3) natural vegetation canopies. Morgan and Smith (1976, 1978) have described the development of C. album in response to low red:far-red ratio. Previously, several workers (Kasperbauer, 1971; Fitter and Ashmore, 1974; Young, 1975; Frankland and Letendre, 1978) have attempted to relate plant response in nature to either fluence rate, red: far-red ratio or both. Their observations will be discussed below. MATERIALS AND METHODS 1. Light measurement and zeta Fluence rate and red:far-red ratio were measured with a Gamma Scientific (San Diego) spectroradiometer. In the controlled environment the total fluence rate between 400 nm and 700 nm of white light available for photosynthesis (i.e. photosynthetically active radiation, or PAR) was checked and adjusted using a Lambda Instruments (Lincoln, Nebraska) Quantum Meter. Zeta is the photon fluence rate ratio of red to far-red light in 10 nm bandwidths centred on 660 nm and 730 nm: Fluence rate (/tmol m~^ s~^) nm Fluence rate {fimox m~^ s~^) nm These data are taken from a 400 to 800 nm spectral photon distribution provided by the spectroradiometer. 2. Controlled environment Plant tissue and pretreatment conditions. Seeds of Chenopodium album L., collected from arable land, were germinated on blotting paper. The seedlings were
3 Development of Chenopodium album in shadelight 241 grown in 63-5 mm pots in a pretreatment environment of 16h:20 C day and 8h:15 C night. White light for photosynthesis was from a bank of Phillips 1200 mm 80 W 'warm white' fluorescent tubes, which provided a fluence rate between 400 nm and 700 nm of 180/^mol m~^ s~^ The ^ was Plants were transferred to treatment when the third true leaf-pair was just expanding. Treatment conditions. The same photo- and thermo-period were used; 16h:20 C day and 8h:15 C night. Background white light was provided by either a bank of Phillips 1200 mm 80 W 'warm white' fluorescent tubes or a bank of Osram-GEC 600 mm 40 W 'colour matching' fluorescent tubes. The fluence rate between 400 nm and 700 nm could be varied between 25 and 250/^moJ m"^ s"^ The red.far-red ratio was varied by adding supplementary far-red light to the background white light for the whole of the daily light period. Far-red light was provided by water-cooled Osram-GEC 150 W tungsten bulbs in combination with a broadband far-red filter which has been described previously (Morgan and Smith, 1978). This arrangement allowed ^to be varied between 9 0 and Natural environment Experiment 1. Four 3 x 3 m stands of Nicotiana rustica with 0 3, 0*5 and 07 m plant spacing were grown on arable land at Sutton Bonington. Each stand was bordered by a guard row of plants spaced at 0*5 m intervals. All of the plants were regularly decapitated to maintain a stand height of 1 m. The stands ran in an east-west strip in the order: 07 m; 0-3 m; 0*5 m. A no-canopy control plot was situated at the east end of the tobacco stands. Nine plants of C. album, grown to 120 mm tall in a glasshouse, were planted at random into each of the 4 experimental plots. They were harvested after 27 days; the tobacco was harvested 3 days later. Experiment 2. A single site was selected for three natural light environments, (i) Arable land/no canopy; Sutton Bonington (SK ). (ii) Grass-sward; Sutton Bonington (SK ). A fairly open sward, 250 to 300 mm tall, of evenly mixed Lolium perenne and Agrostis gigantea. Flowering spikes of these grasses formed a thin layer above the main sward, (iii) Woodland; Domleo Spinney (SK ). The canopy cover consisted of 30% Quercus robur, 30% Acer pseudoplatanus, 10 o Fraxinus excelsior and 30% Corylus avellana, with an understorey cover of 5 "o C. avellana and 5% A. pseudoplatanus. Eighteen plants of C. album were grown in a glasshouse until they were placed, still in their 63*5 mm pots, at random under each of the canopies. The plants were watered daily in plots (ii) and (iii), and twice daily in (i). Nine plants were harvested from each environment after 9 days and 21 days. RESULTS AND DISCUSSION 1. The relationship betweenfluencerate, zeta, and the density of a vegetational canopy Figure 1 shows the relationships between fluence rate and leaf area index, and C, and leaf area index for the tobacco canopies described in the materials and methods. Both fluence rate and C, decrease exponentially with increasing leaf area index (canopy density). A similar relationship for ^ and leaf area index under a monocot canopy has been observed by Holmes and Smith (1977b). With such
4 242 D. C. MORGAN AND H. SMITH similar relationships it is impossible to determine from field observations alone which factor may be inducing the developmental changes that occur in shade. 2. Development in response to low fluence rate White fluorescent light with a ^ of 9-02 was used to grow plants for 9 days in a controlled environment. Nine replicate plants were placed in each of the four fluence rates used: 43; 76; 100; and214/*mol m"^ s~^ between 400 nm and 700 nm Leaf area index Fig. 1. The relationships between fluence rate (400 to 700 nm) and leaf area index, and ^ and leaf area index for a tobacco canopy. The sky was overcast. 9, fluence rate; O, ^. Table 1. Effect of a range of fluence rates on development in Chenopodium album Fluence rate ( nm; //mol s~') Dry wt (g) 0-059± Height (mm) 46-2± ± ± ±2-5 Specific stem length (mm mg-') 3-25± ±016 l-82±0-09 l-04±0-06 Specific leaf area (mm mg-') 55-2±l ± ±l-l 29-1 ±1-4 Data are mean + standard error. The highest fluence rate (214/^mol m ^ s ^) is not comparable with midsummer daylight, but it is near the photosynthetic light saturation point for these plants (Morgan, 1977). With decreasing fluence rate there was a large reduction in dry wt and a large increase in specific leaf area (Table 1). The latter is a characteristic response to low irradiance (Blackman and Wilson, 1951, 1954). Stem extension is apparently quite insensitive to low fluence rates - there is only a small reduction in final height - and this contrasts markedly with the large increase in stem extension shown in response to low red:far-red ratio (Morgan and Smith, 1976). However, there is a large change in specific stem length (Table 1). Grime and Jeffrey (1965) found that stem extension could be increased or decreased by low fluence rates. These different reactions were not clearly related
5 Development of Chenopodium album in shadelight 243 to a species habitat but depended on the sites available for extension, and the efficiency of photosynthesis at low fluence rate. 3. Development in response to a combination of low fluence rate and low red.far-red ratio Depending on uniformity, between 9 and 15 plants were grown for 9 days under a range of fluence rates (25 to 100/^mol m"^ s"^ 400 to 700 nm) and ratios of red:far-red light (^ 015 to 426) in the controlled environment. These treatments had little effect on leaf area [Fig. 2(a)]. A large increase in specific leaf area was observed for plants grown in low fluence rates, irrespective of the value of ^. The red:far-red ratio had no effect on this response [Fig. 2(b)]. However, both fluence rate and red:far-red ratio have been shown to affect leaf area in Rumex obtusifolius (McLaren and Smith, 1978), and specific leaf area in Veronica persica (Fitter and Ashmore, 1974) and Impatiens parviflora (Young, 1975). It is probable that the degree to which either of these two environmental factors affect leaf development, and probably development as a whole, is species specific. In C. album, the red:far-red ratio and fluence rate interact to control stem development. Low red: far-red ratios induce a large increase in stem extension rate. (a) 40 E o D D a> Q ~ ~ ~ -A 0 00 (b) 1 i 1 1 (d) o k- o D ~oo ~ ~ ^ ~ 7-0 E A - -A o (U a CO 20 F * Zeta _1 _ _ 4-0 Fig. 2. The relationships between C. and (a) leaf area, (b) specific leaf area, (c) stem extension rate and (d) the leaf dry wt: stem dry wt ratio for C. album grown under a range of fluence rates. Fluence rates: A, 25 /imol m~'^ s"'; O, 45 //mol m"* s~'; and #, 100//mol m~'^ s"'. Each point represents the mean of between 9 and 15 replicate plants.
6 244 D- C. MORGAN AND H. SMITH but this response is decreased at low fluence rates [Fig. 2(c)]. The leaf dry wt: stenn dry wt ratio decreases with decreasing fluence rate when the red:far-red ratio is high. At a low red:far-red ratio, fluence rate does not affect the leaf dry wt:stem dry wt ratio [Fig. 2(d)]. Warrington, Mitchell and Halligan (1976) demonstrated interaction between fluence rate, temperature, and light quality in the control of development in a series of crop plants. The light quality varied in the ratio of red to blue light as well as in the ratio of red to far-red light, but the range of red: far-red ratio was small. Nevertheless, in Sorghum a similar interaction between fluence rate and red: far-red ratio was shown for the control of plant height, at both high and low temperatures. 4. Development in natural light environments In two separate experiments, plants of C. album were grown beneath a range of planted tobacco canopies, and beneath a range of natural canopies (woodland, grass-sward, and daylight control). The light environments are characterized for the former in Figure 1 and for the latter in Table 2. Figure 3 shows the height time-courses. The kinetics are similar for plants Table 2. Description of the light environment for the natural canopies Fluence rate ( nm; //mol m~^ s~') ^ Mean Range Mean Range Daylight control M Grass-sward Woodland Number of observations: daylight control, 2; grass-sward, 4; woodland, 4. growing beneath both tobacco and natural canopies. Beneath the deepest shade [tobacco 0-5 m. Figure 3(a); woodland. Figure 3(b)] the plants grew rapidly for a short time, and quickly exceeded the height of the daylight controls. Soon (after 2 to 5 days), however, the stem extension rate of the plants in shade decreased, and the daylight controls became taller. Those plants which grew beneath less dense canopies [tobacco 0-7 m. Figure 3(a); grass-sward. Figure 3(b)] also showed rapid initial extension, but this was maintained for longer. By day 9 the C. album plants had overtopped the grass-sward canopy. Aerial dry wt and leaf dry wt: stem dry wt ratio decreased with increasing canopy density for plants growing beneath the tobacco canopy [Table 3(a)], and speciflc leaf area increased with increasing canopy density for plants growing beneath both the tobacco [Table 3(a)] and natural [Table 3(b)] canopies. An increase of speciflc leaf area is characteristic for plants growing beneath vegetational canopies. It has been observed in Impatiens parviflora (Coombe, 1966) and Circaea lutetiana (Frankland and Letendre, 1978) growing beneath oak woodland, and in Veronica persica and V. montana (Fitter and Ashmore, 1974) growing beneath a tobacco canopy. Frankland and Letendre (1978) also observed that the flnal height in C. lutetiana was reduced for plants growing in the shade.
7 Development of Chenopodium album in shadelight k E Time (days) Fig. 3. Height-time course for C. album plants grown under vegetational canopies, (a) Tobacco canopies:, daylight control;, 0 7m spacing; and A, 05 m spacing. Light environment described in Eigure 1. (b) Natural canopies:, daylight control;, grass-sward; and A, woodland. Light environment described in Table 2. Bars show ± standard error. 5. Detection of fluence rate and red: far-red ratio by plants growing in nature The development patterns which have been observed for plants growing beneath vegetational canopies may result from the light environment, but such interpretation must be viewed with caution. Humidity, mechanical stress (wind speed) and temperature are all affected by vegetational shade, and these may also affect plant development. Stem extension in Liquidambar is reduced in plants which have been subjected to mechanical stress (Neel and Harris, 1971). Specific leaf area is affected by temperature, rooting medium and daylength, as well as being subject to ontogenetic drift (Young, 1975). Nevertheless, the relationships between
8 246 D. C. MORGAN AND H. SMITH Table 3. Aerial dry weight and specific leaf area for Chenopodium album plants growing under vegetational canopies, (a) Tobacco canopies; light environment described in Figure 1. (b) Natural canopies; light environment described in Table 2 (a) Tobacco Canopy spacing (m) control Aerial dry weight (g) Specific leaf area (mm mg~') 0-94 ± ± ± ± ± ±0-9 (b) Natural canopies Canopy M Daylight control Grass-sward Woodland Aerial dry weight (g) day 21 Specific leaf area (mm mg~') (i) day 9 (ii) day ± ± ± ± ± ± ±2-3 Stem extension and canopy density, and specific leaf area and canopy density are entirely consistent with the effects of controlled environment lighting regimes. Often, however, it has not been possible to distinguish the effects of low red: far-red ratio and low fiuence. Kasperbauer (1971) observed that leaf shape was similarly affected by low red:far-red ratio in the controlled environment and by vegetational shade. The effect of low fiuence rate, which is known to change leaf morphology (Hughes, 1959), was not considered. Fitter and Ashmore (1974) found that low fluence rate and low red: far-red ratio resulted in a reduction of leaf area in the shade-intolerant Veronica persica, for plants growing in the controlled environment, but whether the reduction of leaf area observed under vegetational shade was due to either or both could not be determined. The developmental pattern shown by Circaea lutetiana growing under vegetational shade was most closely simulated in the controlled environment by low fiuence rate alone; low red:far-red ratio had no effect (Frankland and Letendre, 1978). However, Circaea lutetiana is a woodland plant which has been show^n to be less responsive to red:far-red ratio than shade-intolerant species (Morgan and Smith, 1979), and furthermore these plants were not given the full natural range of red:far-red ratio. Fluence rate was found to determine specific leaf area in Chenopodium album in the experiments described above; in low fiuence rates specific leaf area was large [Fig. 2(b)]. Similarly, specific leaf area increased with decreasing fiuence rate for plants grown under the vegetational canopies. The change in specific leaf area between 9 and 21 days for C album growing in the grass-sward may refiect the higher fiuence rate these plants received when the canopy had been overtopped. Young (1975) has shown that the increase in specific leaf area which Impatiens parviflora shows under vegetational shade may be accounted for by the combined effect of low fiuence rate and low red:far-red ratio. Stem extension in C. album growing in the controlled environment, was only increased by low red:far-red ratio; low fiuence rate reduced this response. For
9 Development of Chenopodium album in shadelight 247 plants growing beneath the vegetation canopies, the initial enhanced stem extension rate may have been due to the low red: far-red ratio and the subsequent reduced extension rate for plants growing in the deepest shade may have resulted from the low fluence rate, perhaps because of a reduction in the photosynthate available for growth. The extremely rapid initial extension shown by the plants growing in grass-sward did not subsequently decline. This may reflect the sensitivity to a change in red:far-red ratio which this species shows when it is growing under a sufliciently high fluence rate [Fig. 2(c); 100 /^mol m'^ s^i]. These plants overtopped the grass-sward and accumulated the largest aerial dry wt [Table 3(b)]. The data indicate that for ruderal species, with short life histories, the stem extension response to low red: far-red ratio, for which there is strong evidence to suggest control by phytochrome, is of considerable ecological signiflcance. In these plants the production of numerous seeds, which is linked to dry wt accumulation, is critical for species survival. Species from other habitats, with contrasting life histories, also respond to changes in the red:far-red ratio (Morgan and Smith, 1979), but the ecological significance of the response for these species will not be fully appreciated without further fleld experimentation. ACKNOWLEDGEMENTS The authors wish to thank John Topham and Martin Crawford for their assistance with the fleld experiments. This work was flnancially supported by the NERC. REFERENCES BjORKMAN, O. (1968a). Carboxydismutase activity in shade- and sun-adapted species of higher plants. Physiotogia Ptantarum, 21, BjORKMAN, O. (1968b). Further studies on differentiation of photosynthetic properties in sun and shade ecotypes of Sotidago virgaurea. Physiotogia Ptantarum, 21, BLACKMAN, G. E. & WILSON, G. L. (1951). Physiological and ecological studies in the analysis of plant environment. VII. An analysis of the differential effects of light intensity on NAR, LAR and RGR of different species. Annats of Botany N.S., 15, BLACKMAN, G. E. & WILSON, G. L. (1954). Physiological and ecological studies in the analysis of plant environment. IX. Adaptive changes in the vegetative growth and development of Hetianthus annuus induced by an alteration in light level. Annats of Botany N.S., 18, COOMBE, D. E. (1966). The seasonal light climate and plant growth in a Cambridgeshire wood. In: Light as an Ecotogicat Factor {Ed. hy R. Bainbridge, E. Clifford Evans & O. Rackham), pp Blackwell Scientific Publications, Oxford. FITTER, A. H. & ASHMORE, C. J. (1974). Response of two Veronica species to a simulated woodland light climate. New Phytologist, 73, FRANKLAND, B. & LETENDRE, R. J. (1978). Phytochrome and effects of shading on the growth of woodland plants. Photochemistry and Photobiotogy, 27, GRIME, J. P. & JEFFREY, D. W. (1965). Seedling establishment in vertical gradients of sunlight. Journat of Ecotogy, 53, HOLMES, M. G. & SMITH, H. (1975). The function of phytochrome in plants growing in the natural environment. Nature, 254, HOLMES, M. G. & SMITH, H. (1977a). The function of phytochrome in the natural environment. I. Characterisation of daylight for studies in photomorphogenesis and photoperiodism. Photochemistry and Photobiology, 25, HOLMES, M. G. & SMITH, H. (1977b). The function of phytochrome in the natural environment. II. The influence of vegetation canopies on the spectral energy distribution of natural daylight. Photochemistry and Photobiotogy, 25, HOLMES, M. G. & SMITH. H. (1977C). The function of phytochrome in the natural environment. IV. Light quality and plant development. Photochemistry and Photobiotogy, 25, HUGHES, A. P. (1959). Effects of the environment on leaf development in Impatiens parzifiora D.C. Journal of the Linnean Society, 56,
10 248 D. C. MORGAN AND H. SMITH JARVIS, P. G. (1964). The adaptability to light intensity of seedlings of Quercus patraea. Journal of Ecology 52, KASPERBAUER, M. J. (1971). Spectral distribution of light in a tobacco canopy and eftect of end-of-day light quality on growth and development. Plant Physiology, 47, MCLAREN, J. S. & SMITH, H. (1978). Phytochrome control of the growth and development of Rumex obtusifolius under simulated canopy light environments. Plant, Cell and Environment, 1, MONTEITH, J. L. (1976). Spectral distribution of light in leaves and foliage. In: Light and Plant Development (Ed. by H. Smith), pp Butterworths, London. MORGAN, D. C. (1977). The function of phytochrome in the natural environment. Ph.D. Thesis, University of Nottingham. MORGAN, D. C, O'BRIEN, T. & SMITH, H. (1980). Rapid photomodulation of stem extension in light-grown Sinapis alba L.: studies on kinetics, site of perception and photoreceptor. Planta, 150, MORGAN, D. C. & SMITH, H. (1976). Linear relationship between phytochrome pbotoequilibrium and growth in plants under simulated natural radiation. Nature, 262, MORGAN, D. C. & SMITH, H. (1978). The relationship between pbytocbrome photoequilibrium and development in light grown Chenopodium album L. Planta, 142, MORGAN, D. C.& SMITH, H.( 1979). A systematic relationship between pbytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta, 145, NEEL, P. L. & HARRIS, R. W. (1971). Motion-induced inhibition of elongation and induction of dormancy in Liquidambar. Science., 173, SMITH, H. & HOLMES, M. G. (1977). The function of phytochrome in the natural environment. III. Measurement and calculation of phytochrome pbotoequilibrium. Photochemistry and Photobiology, TASKER, R. & SMITH, H. (1977). The function of pbytochrome in the natural environment. V. Seasonal cbanges in the radiant energy quality in woodlands. Photochemistry and Photobiology, 26, 487^91. VEZINA, P. E. & BOULTER, D. W. K. (1966). The spectral composition of near U.V. and visible radiation beneatb forest canopies. Canadian Journal of Botany, 44, WARRINGTON, I. J., MITCHELL, K. J. & HALLIGAN, G. (1976). Comparisons of plant growth under four different lamp combinations and various temperature and irradiance levels. Agricultural Meteorology, 16, YocuM, C. S., ALLEN, L. H. & LEMON, E. R. (1964). Photosynthesis under field conditions: VI. Solar radiation balance and photosynthetic efficiency. Agronomy Journal, 56, YOUNG, J. E. (1975). Effects of the spectral composition of light sources on tbe growth of a higher plant. In: Light as an Ecological Factor II (Ed. by G. Clifford Evans, R. Bainbridge & O. Rackbam), pp , Blackwell Scientific Publications, Oxford.
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